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osseointegration has a predominant fibrous tissue contraindications to implant placement, several factors
capsule, preventing direct contact between implant and may contribute to implant loss and the reaction of peri-
bone and resulting in impaired implant function. Other implant tissues. The primary etiology of biological
biological implant complications, which occur more implant complications is bacterial infection. The
commonly, are peri-implant diseases. Peri-implant microbial profile of peri-implant disease is complex. In
diseases are comprised of peri-implantitis and peri- spite of the diversity, the most predominant species are
implant mucositis, which are characterized by the Gram-negative anaerobic bacteria (Mombelli and
presence or absence of bone loss, respectively. In the Decaillet, 2011). Unlike the microbiota of successful
consensus reports of the Sixth European Workshop on osseointegrated implants (Lee et al., 1999), periodontal
Periodontology (6th EWOP), “peri-implant mucositis” pathogens (from both the orange and red complex)
was defined as inflammatory lesions limited to the have been predominantly associated with peri-implant
mucosa, whereas the lesions in “peri-implantitis” sites diseases (Al-Radha et al., 2012; Charalampakis et al.,
extend to supporting bone (Lindhe and Meyle, 2008). 2012). In a recent study by Al-Radha and coworkers, 22
Recently, the 7th EWOP has confirmed that the key patients with signs of peri-implant disease were
diagnostic feature of peri-implant mucositis is the evaluated and there was reportedly a positive
presence of bleeding on probing when using a force correlation between the percentage of red complex
<0.25 Newtons. Moreover, the essential parameter for bacteria and the severity of disease (i.e., pocket depth
the diagnosis of peri-implantitis is evidence of and gingival index; Al-Radha et al., 2012). In addition to
progressive bone loss at the site of the implant (Lang microbiota, environmental factors including plaque and
and Berglundh, 2011). However, clinicians should individual susceptibility (Dereka et al., 2012; Mombelli
remember to distinguish inflammation-induced bone and Decaillet, 2011), smoking (Bain and Moy, 1993; De
loss from biological bone remodeling when diagnosing Boever et al., 2009; DeLuca et al., 2006; Vervaeke et al.,
peri-implantitis. Table 2 summarizes the definitions and 2012), systemic diseases/past head and neck radiation
the clinical characteristics of both peri-implant (Anderson et al., 2013; Marchand et al., 2012; Moy et al.,
mucositis and peri-implantitis. 2005; Oates et al., 2009; Yerit et al., 2006), and
The incidence of implant loss varies from the type periodontal stability (De Boever et al., 2009) all can
of prosthesis, location, and timing of implant loss. potentially influence the healing capacity of the host
From a meta-analysis including studies with more than and ultimately affect the incidence of implant loss.
five years follow-up, the reported rate of implant loss Another factor to consider is bone density, as implants
prior to function was 2.16-2.53%. In the late stage, the placed in type IV bone are more prone to failure than
incidence of implant loss was 2-3% and >5% with those placed in type I bone (Goodacre et al., 2003).
implant-supported fixed prosthesis and overdentures, Next, implant-related factors include considerations
respectively (Berglundh et al., 2002). In addition, higher such as implant length and diameter (Alsaadi et al., 2008;
survival rates were reported in implants placed in Baqain et al., 2012; Chung et al., 2007; Monje et al., 2012),
partially edentulous patients compared with those in and even modification of implant design has been
fully edentulous ridges (Esposito et al., 1998; Goodacre introduced to control the effects of the microgap and
et al., 2003). A higher incidence of implant loss was minimize the reestablishment of biological width (Oh et
observed in the maxilla in cases of patients who were al., 2002; Tatarakis et al., 2012). Moreover, peri-implant
treated with a full-arch prosthesis (Goodacre et al., bone loss may result from surgical trauma (Eriksson and
2003). The incidence of peri-implant diseases varies Albrektsson, 1984; Oh et al., 2002) and implant
from that reported in some previous literature because malpositioning (Evans and Chen, 2008; Hermann et al.,
of a lack of consistent criteria/definition. The 2000). Another important restorative/iatrogenic factor
prevalence of peri-implant mucositis ranges from is residual cement. Among 42 implants with signs of
38.9% to 90.9% (Fransson et al., 2008; Rinke et al., 2011). peri-implant disease, Wilson found that 80.95% of the
Similarly, bone loss has been reported in 10% - 28% of cases were associated with residual cement. The
implants during various experimental periods resolution of the clinical and endoscopic signs was
(Fransson et al., 2008; Karoussis et al., 2004). An observed in most of the cases (76%) 30 days after the
example may explain how the definition of disease cement was removed (Wilson, 2009).
affects the prevalence. To c o n t r o l i n f l a m m a t i o n a n d r e g a i n
In 1999, Roos-Jansaker and co-workers reported osseointegration, several decision trees have been
that the incidence of peri-implantitis was 16% by their proposed. In 1997, Lang and coworkers published a
definition, i.e., more than 1.8 mm bone loss (e.g., 3 decision tree, named “Cumulative Interceptive
threads in the Branemark system) following the first Supportive Therapy (CIST).” In this chart, the
year of function, although their results showed >56% treatment decision is based on the pocket depth, plaque
of implants demonstrating bone loss ≥1 threads with index, morphology of defects and the presence of BOP
or without bleeding on probing (BOP; Roos-Jansaker (Lang et al., 1997). Later, a flow chart was suggested by
et al., 2006). Mombelli. In this flow chart, the treatment is given
Even though there are minimal absolute according to the findings from clinical and radiographic
Yung-Ting Hsu et al.: Management of biological implant complications 11
examination and microbial tests (Mombelli, 2002). In and colleagues (2011). Although the authors reported
2011, Okayasu and Wang recommended a decision tree improved BOP scores with the air-abrasive device, the
for the management of peri-implant diseases. For the reductions in probing depth (PD) were less than 0.6 mm
first time, the amount of bone loss was proposed to be a (Sahm et al., 2011).
critical factor in determining treatment strategies In contrast, positive outcomes have been
(Okayasu and Wang, 2011). More recently, Aljateeli and demonstrated with treatment of peri-mucositis utilizing
colleagues recommended another decision tree to mechanical therapy. In both animal and human studies,
manage “peri-implant bone loss” (Aljateeli et al., 2012). research suggests that mechanical debridement alone is
In this decision tree, both etiology and defect effective in controlling peri-implant mucositis in terms
morphology were taken into consideration. Thus, it of PD reduction, clinical attachment loss (CAL) gain,
should be noticed that this is a guideline for the plaque reduction and control of inflammation.
treatment of not only biological but also biomechanical However, the results of these studies did not lend
implant complications. This purpose of this manuscript support to the additional benefit of adjunctive
is to provide a guideline for the management of antiseptic therapy in conjunction with mechanical
biological implant complications. In addition, common treatment (Porras et al., 2002; Trejo et al., 2006).
biological implant complications are discussed as well as As an adjunct therapy to mechanical debridement,
a review of the currently available treatment strategies. local and systemic antibiotics have also been evaluated.
Compared with chlorhexidine gel, significantly better
Decision tree: the management of biological outcomes have been observed with the use of
implant complications minocycline microspheres for the treatment of peri-
Focusing on the management of biological implant implant diseases. Additionally, the authors claimed that
complications (i.e., implant loss, peri-implant mucositis repeated antimicrobial therapy sustained the PD
and peri-implantitis), a decision process is proposed in reduction and the level of microbial pathogens up to 12
Figure 1. In addition to accurate diagnosis of the months following treatment. Nevertheless, the mean
etiologic factors, the treatment modalities should be PD reduction in the deepest pockets was 0.6 mm at 12
chosen based on the severity of peri-implant diseases, months in both the single and repeated antibiotic
amount of bone loss and the morphology of peri- delivery groups (Renvert et al., 2006; Renvert et al.,
implant bony defects. 2008). Significant but minimal benefits on probing
In order to control the inflammation and stop attachment loss (PAL) gains (0.6 mm) were also
disease progression, numerous nonsurgical and surgical observed with the use of doxycycline hyclate gel
treatments have been proposed. To gain additional (Buchter et al., 2004). On the other hand, limited studies
benefits, adjunctive therapy may be given such as have been conducted that investigate the effects of
antiseptics, or local and/or systemic antibiotics, as well systemic antibiotics. In terms of reduction of bleeding
as application of laser therapy. It should be kept in mind index and PD, the use of ornidazole appeared to be
that it is difficult to compare the results of many of effective, as was reported in a case series (n = 9) with
these studies because of the heterogeneity of nine implants that had a 12-month follow-up (Mombelli
experimental designs and the diverse definitions of and Lang, 1992). A recent randomized clinical trial with
peri-implant diseases that were used throughout the a larger sample size failed to show any benefit of
literature. Thus, clinicians should remember and take systemic azithromycin administration in the treatment
note of the clinical significance and potential of peri-implant mucositis (Hallstrom et al., 2012). Based
applications of these treatments when interpreting on the scarcity of data that are currently available, more
these data. studies are needed to provide conclusive evidence
regarding the effects of adjunctive systemic antibiotics
Non-surgical approaches for the treatment of peri-implant diseases.
In recent years, the application of laser therapy has
To disrupt the biofilm around implants, mechanical been introduced to treat peri-implant diseases. Without
debridement has been applied using hand instruments, surgical approaches, some studies were conducted to
sonic instruments, ultrasonic instruments and air- compare the effects of laser devices with mechanical
abrasive devices. For the treatment of peri-implantitis, a debridement. A series of studies published by Schwarz
double-blinded randomized trial was conducted by and coworkers evaluated the non-surgical treatment
Renvert and co-workers (2009). Thirty-one patients outcomes of Er:YAG laser treatment within 12 months.
were enrolled in the study and infected implants were In spite of significant improvement in BOP reduction
treated using either titanium curettes or ultrasonics. during the experimental periods, the laser application
Although there was improvement in plaque and only exhibited significant CAL gain at 3 and 6 months
bleeding scores, both treatment modalities failed to post-operatively compared with baseline. However,
reduce pocket depth or bacterial counts during the 6- there were no significant differences in PD or CAL
month experimental period (Persson et al., 2010; changes between laser-treated and control (mechanical
Renvert et al., 2009). The minimal effectiveness of debridement using plastic curettes in combination with
mechanical debridement was also confirmed by Sahm
12 Journal of the International Academy of Periodontology 2014 16/1
Table 2. The definitions and the clinical characteristics of both peri-implant mucositis and peri-implantitis
0.2% chlorhexidine (CHX) irrigation) groups at any of resective therapy for peri-implantitis. In the
timepoint (Schwarz et al., 2006a; Schwarz et al., 2005). comparative studies published by Romeo and co-
The result was further confirmed by later studies researchers (2005, 2007), implantoplasty groups
comparing the use of the Er:YAG laser with an air- exhibited higher implant survival rates and less alveolar
abrasive device (Persson et al., 2011; Renvert et al., 2011). bone loss over the 3-year experimental periods. Better
In regards to microbiological changes, a single episode clinical results (lower PD, PAL and modified bleeding
of laser application may reduce the counts of index) were also observed at the sites with surface
Fusobacterium nucleatum naviforme and Fusobacterium modification (Romeo et al., 2005; Romeo et al., 2007). As
nucleatum nucleatum within one month after therapy. for concerns of thermal changes during implantoplasty,
Nevertheless, the antimicrobial effects failed to be an in vivo study indicated that minimal temperatures
maintained at the 6-month follow-up time point (approximately 1.5ºC) were generated during
(Persson et al., 2011). implantoplasty with a properly selected bur and cooling
system (Sharon et al., 2011).
Surgical approaches In addition to resective procedures, regenerative
In the treatment of peri-implantitis, surgical approaches therapy is another treatment modality to re-establish
appear to be a predictable method over a short-term osseointegration around a dental implant. Before any
period (Renvert et al., 2012). In general, surgical therapy regenerative procedures can work, a surface
consists of access flap surgery, degranulation and detoxification must be done first. Decontamination of
decontamination of the implant surface. To gain access the implant surface can be performed by way of several
and facilitate home care, resective surgery is performed methods. Similar to non-surgical mechanical
either alone or in conjunction with implant surface debridement, the main g oal of mechanical
modification (implantoplasty). In contrast, regenerative decontamination is to rupture the implant biofilm.
procedures should be considered to regenerate bone In addition, chemical modalities have been
(Renvert et al., 2012). introduced to suppress bacterial load in peri-implantitis
Resective surger y consists of an apically sites. They include hydrogen peroxide (Roos-Jansaker et
repositioned flap (APF) along with bone re-contouring, al., 2011; Roos-Jansaker et al., 2007b), saline (Behneke et
which ultimately leads to pocket reduction. With a 2- al., 2000; Schwarz et al., 2008), 35% phosphoric acid gel,
year follow-up, Serino and Turri (2011) reported CHX (Hammerle et al., 1995; Khoury and Buchmann,
positive outcomes of resective treatment on 86 2001; Wiltfang et al., 2012), citric acid (Khoury and
implants with peri-implantitis. In addition, more Buchmann, 2001), and EDTA (Roccuzzo et al., 2011).
implants (74%) with a minimal amount of initial bone Another choice for implant surface decontamination is
loss (2-4 mm) returned to healthy status (no signs of laser application, such as the CO2 laser (Deppe et al.,
peri-implant diseases) compared to those implants with 2007; Romanos and Nentwig, 2008), the diode laser
>5 mm initial bone loss (40%; Serino and Turri, 2011). (Bach et al., 2000) and the Er:YAG laser (Schwarz et al.,
Without implantoplasty, a recent double-blind 2011b). Despite decontamination modalities that have
randomized controlled trial evaluated the effects of been widely applied in combination with surgical
resective surgery with surface debridement on a total of treatments, some authors questioned the effects of
79 implants from 30 patients. Significant clinical these procedures. In a recent meta-analysis, Renvert and
improvements in terms of PD and BOP reduction were c owo r ke r s r e f u t e d t h e b e n e f i t s f r o m l a s e r
observed over a 12-month follow-up time period (de decontamination (Renvert et al., 2012). Compared with
Waal et al., 2013). On the contrary, some authors those who received conventional mechanical
proposed that implantoplasty may augment the benefits debridement (plastic curettes), the laser-treated group
14 Journal of the International Academy of Periodontology 2014 16/1
did not exhibit better inflammation control (i.e., higher osseointegration, decontamination of implant surfaces
BOP reduction and CAL gain) in the treatment of via chemical or mechanical techniques are still the most
advanced peri-implantitis (Schwarz et al., 2011a). With highly recommended (Subramani and Wismeijer, 2012).
resective surgery, the CHX/cetylpyridinium chloride To date, there is no consensus on the indications and/or
(CPC) group achieved greater reduction of bacterial criteria for when to perform peri-implant regeneration.
load, but failed to show any clinical superiority when From the criteria of case selection in previous studies,
compared to the control group (without CHX/CPC; de the defect types that have been suggested include crater-
Waal et al., 2013). However, it is difficult to compare the like or saucer-shaped defects (Behneke et al., 2000;
effects of different treatment modalities because more Roccuzzo et al., 2011; Wiltfang et al., 2012), intrabony
than one decontamination method has been used in defects with 3 mm depth (Schwarz et al., 2006b;
most studies. Furthermore, systemic antibiotics were Schwarz et al., 2008) and >3 threads of progressive loss
given in most of the studies. To reach optimum re- (Roos-Jansaker et al., 2011; Schwarz et al., 2011b). As is
Yung-Ting Hsu et al.: Management of biological implant complications 15
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18 Journal of the International Academy of Periodontology 2014 16/1